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The Metallo-β-Lactamase Family of Ribonucleases

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Ribonucleases

Part of the book series: Nucleic Acids and Molecular Biology ((NUCLEIC))

Abstract

The metallo-β-lactamases (MβLs) constitute a very ancient family of enzymes with a wide range of substrates, including RNA and DNA. The β-lactamases that act on RNA (here called rMβLs) can be grouped into two major families, the RNase Z family and the β-CASP family. Members of the RNase Z family are primarily involved in the maturation of the 3′ end of tRNAs, whereas members of the β-CASP family have thus far been shown to have primarily mRNA and snRNA targets. Although they share a metallo-β-lactamase core and catalytic mechanism, the two families are easily distinguishable at the sequence level and by the presence of characteristic subdomains that play a key role in substrate recognition. These are principally the so-called flexible arm (about 40 amino-acids) of RNase Z and the β-CASP domain (>160 amino-acids) that gives its name to this family of enzymes. In this chapter, I will describe our current understanding of these two MβL families, with particular emphasis on their structures, their substrates, and their phylogenic distribution.

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References

  • Ach RA, Weiner AM (1987) The highly conserved U small nuclear RNA 3′-end formation signal is quite tolerant to mutation. Mol Cell Biol 7(6):2070–2079

    PubMed  CAS  Google Scholar 

  • Aravind L (1999) An evolutionary classification of the metallo-beta-lactamase fold proteins. In Silico Biol 1(2):69–91

    PubMed  CAS  Google Scholar 

  • Asha PK, Blouin RT, Zaniewski R, Deutscher MP (1983) Ribonuclease BN: identification and partial characterization of a new tRNA processing enzyme. Proc Natl Acad Sci USA 80(11):3301–3304

    Article  PubMed  CAS  Google Scholar 

  • Baillat D, Hakimi MA, Naar AM, Shilatifard A, Cooch N, Shiekhattar R (2005) Integrator, a multiprotein mediator of small nuclear RNA processing, associates with the C-terminal repeat of RNA polymerase II. Cell 123(2):265–276

    Article  PubMed  CAS  Google Scholar 

  • Britton RA, Wen T, Schaefer L, Pellegrini O, Uicker WC, Mathy N, Tobin C, Daou R, Szyk J, Condon C (2007) Maturation of the 5′ end of Bacillus subtilis 16 S rRNA by the essential ribonuclease YkqC/RNase J1. Mol Microbiol 63(1):127–138

    Article  PubMed  CAS  Google Scholar 

  • Bugrysheva JV, Scott JR (2010) The ribonucleases J1 and J2 are essential for growth and have independent roles in mRNA decay in Streptococcus pyogenes. Mol Microbiol 75(3):731–743

    Article  PubMed  CAS  Google Scholar 

  • Callebaut I, Moshous D, Mornon JP, de Villartay JP (2002) Metallo-beta-lactamase fold within nucleic acids processing enzymes: the beta-CASP family. Nucleic Acids Res 30(16):3592–3601

    Article  PubMed  CAS  Google Scholar 

  • Clouet-d'Orval B, Rinaldi D, Quentin Y, Carpousis AJ (2010) Euryarchaeal beta-CASP proteins with homology to bacterial RNase J have 5′- to 3′-exoribonuclease activity. J Biol Chem 285(23):17574–17583

    Article  PubMed  Google Scholar 

  • Colgan DF, Manley JL (1997) Mechanism and regulation of mRNA polyadenylation. Genes Dev 11(21):2755–2766

    Article  PubMed  CAS  Google Scholar 

  • Connelly S, Manley JL (1988) A functional mRNA polyadenylation signal is required for transcription termination by RNA polymerase II. Genes Dev 2(4):440–452

    Article  PubMed  CAS  Google Scholar 

  • Daiyasu H, Osaka K, Ishino Y, Toh H (2001) Expansion of the zinc metallo-hydrolase family of the beta-lactamase fold. FEBS Lett 503(1):1–6

    Article  PubMed  CAS  Google Scholar 

  • Daou-Chabo R, Condon C (2009) RNase J1 endonuclease activity as a probe of RNA secondary structure. RNA 15(7):1417–1425

    Article  PubMed  CAS  Google Scholar 

  • Daou-Chabo R, Mathy N, Benard L, Condon C (2009) Ribosomes initiating translation of the hbs mRNA protect it from 5′-to-3′ exoribonucleolytic degradation by RNase J1. Mol Microbiol 71(6):1538–1550

    Article  PubMed  CAS  Google Scholar 

  • de Vegvar HE, Lund E, Dahlberg JE (1986) 3′ end formation of U1 snRNA precursors is coupled to transcription from snRNA promoters. Cell 47(2):259–266

    Article  PubMed  Google Scholar 

  • Deikus G, Condon C, Bechhofer DH (2008) Role of Bacillus subtilis RNase J1 endonuclease and 5′-exonuclease activities in trp leader RNA turnover. J Biol Chem 283(25):17158–17167

    Article  PubMed  CAS  Google Scholar 

  • Dominski Z (2007) Nucleases of the metallo-beta-lactamase family and their role in DNA and RNA metabolism. Crit Rev Biochem Mol Biol 42(2):67–93

    Article  PubMed  CAS  Google Scholar 

  • Dominski Z, Marzluff WF (1999) Formation of the 3′ end of histone mRNA. Gene 239(1):1–14

    Article  PubMed  CAS  Google Scholar 

  • Dominski Z, Zheng LX, Sanchez R, Marzluff WF (1999) Stem-loop binding protein facilitates 3′-end formation by stabilizing U7 snRNP binding to histone pre-mRNA. Mol Cell Biol 19(5):3561–3570

    PubMed  CAS  Google Scholar 

  • Dominski Z, Erkmann JA, Yang X, Sanchez R, Marzluff WF (2002) A novel zinc finger protein is associated with U7 snRNP and interacts with the stem-loop binding protein in the histone pre-mRNP to stimulate 3′-end processing. Genes Dev 16(1):58–71

    Article  PubMed  CAS  Google Scholar 

  • Dominski Z, Yang XC, Marzluff WF (2005a) The polyadenylation factor CPSF-73 is involved in histone-pre-mRNA processing. Cell 123(1):37–48

    Article  PubMed  CAS  Google Scholar 

  • Dominski Z, Yang XC, Purdy M, Wagner EJ, Marzluff WF (2005b) A CPSF-73 homologue is required for cell cycle progression but not cell growth and interacts with a protein having features of CPSF-100. Mol Cell Biol 25(4):1489–1500

    Article  PubMed  CAS  Google Scholar 

  • Dutta T, Deutscher MP (2009a) Catalytic properties of RNase BN/RNase Z from Escherichia coli: RNase BN is both an exo- and endoribonuclease. J Biol Chem 284(23):15425–15431

    Article  PubMed  CAS  Google Scholar 

  • Dutta T, Deutscher MP (2009b) Mode of action of RNase BN/RNase Z on tRNA precursors: RNase BN does not remove the CCA sequence from tRNA. J Biol Chem 285(30):22874–22881

    Article  Google Scholar 

  • Even S, Pellegrini O, Zig L, Labas V, Vinh J, Brechemmier-Baey D, Putzer H (2005) Ribonucleases J1 and J2: two novel endoribonucleases in B. subtilis with functional homology to E. coli RNase E. Nucleic Acids Res 33(7):2141–2152

    Article  PubMed  CAS  Google Scholar 

  • Goodarzi AA, Yu Y, Riballo E, Douglas P, Walker SA, Ye R, Harer C, Marchetti C, Morrice N, Jeggo PA, Lees-Miller SP (2006) DNA-PK autophosphorylation facilitates artemis endonuclease activity. EMBO J 25(16):3880–3889

    Article  PubMed  CAS  Google Scholar 

  • Hartmann RK, Gossringer M, Spath B, Fischer S, Marchfelder A (2009) The making of tRNAs and more – RNase P and tRNase Z. Prog Mol Biol Transl Sci 85:319–368

    Article  PubMed  CAS  Google Scholar 

  • Hasenohrl D, Konrat R, Blasi U (2011) Identification of an RNase J ortholog in Sulfolobus solfataricus: implications for 5′-to-3′ directional decay and 5′-end protection of mRNA in Crenarchaeota. RNA 17(1):99–107

    Article  PubMed  Google Scholar 

  • Hernandez N (1985) Formation of the 3′ end of U1 snRNA is directed by a conserved sequence located downstream of the coding region. EMBO J 4(7):1827–1837

    PubMed  CAS  Google Scholar 

  • Hernandez N, Weiner AM (1986) Formation of the 3′ end of U1 snRNA requires compatible snRNA promoter elements. Cell 47(2):249–258

    Article  PubMed  CAS  Google Scholar 

  • Hirose Y, Manley JL (1997) Creatine phosphate, not ATP, is required for 3′ end cleavage of mammalian pre-mRNA in vitro. J Biol Chem 272(47):29636–29642

    Article  PubMed  CAS  Google Scholar 

  • Holzle A, Fischer S, Heyer R, Schutz S, Zacharias M, Walther P, Allers T, Marchfelder A (2008) Maturation of the 5 S rRNA 5′ end is catalyzed in vitro by the endonuclease tRNase Z in the archaeon H. volcanii. RNA 14(5):928–937

    Article  PubMed  Google Scholar 

  • Hunt A, Rawlins JP, Thomaides HB, Errington J (2006) Functional analysis of 11 putative essential genes in Bacillus subtilis. Microbiology 152(10):2895–2907

    Article  PubMed  CAS  Google Scholar 

  • Ishii R, Minagawa A, Takaku H, Takagi M, Nashimoto M, Yokoyama S (2005) Crystal structure of the tRNA 3′ processing endoribonuclease tRNase Z from Thermotoga maritima. J Biol Chem 280(14):14138–14144

    Article  PubMed  CAS  Google Scholar 

  • Ishii R, Minagawa A, Takaku H, Takagi M, Nashimoto M, Yokoyama S (2007) The structure of the flexible arm of Thermotoga maritima tRNase Z differs from those of homologous enzymes. Acta Crystallogr F Struct Biol Cryst Commun 63(8):637–641

    Article  Google Scholar 

  • Ishikawa H, Nakagawa N, Kuramitsu S, Masui R (2006) Crystal structure of TTHA0252 from Thermus thermophilus HB8, a RNA degradation protein of the metallo-beta-lactamase superfamily. J Biochem 140(4):535–542

    Article  PubMed  CAS  Google Scholar 

  • Kaufmann I, Martin G, Friedlein A, Langen H, Keller W (2004) Human Fip1 is a subunit of CPSF that binds to U-rich RNA elements and stimulates poly(A) polymerase. EMBO J 23(3):616–626

    Article  PubMed  CAS  Google Scholar 

  • Kolev NG, Steitz JA (2005) Symplekin and multiple other polyadenylation factors participate in 3′-end maturation of histone mRNAs. Genes Dev 19(21):2583–2592

    Article  PubMed  CAS  Google Scholar 

  • Kostelecky B, Pohl E, Vogel A, Schilling O, Meyer-Klaucke W (2006) The crystal structure of the zinc phosphodiesterase from Escherichia coli provides insight into function and cooperativity of tRNase Z-family proteins. J Bacteriol 188(4):1607–1614

    Article  PubMed  CAS  Google Scholar 

  • Li de la Sierra-Gallay I, Pellegrini O, Condon C (2005) Structural basis for substrate binding, cleavage and allostery in the tRNA maturase RNase Z. Nature 433(7026):657–661

    Article  PubMed  Google Scholar 

  • Li de la Sierra-Gallay I, Mathy N, Pellegrini O, Condon C (2006) Structure of the ubiquitous 3′ processing enzyme RNase Z bound to transfer RNA. Nat Struct Mol Biol 13:376–377

    Article  PubMed  Google Scholar 

  • Li de la Sierra-Gallay I, Zig L, Jamalli A, Putzer H (2008) Structural insights into the dual activity of RNase J. Nat Struct Mol Biol 15(2):206–212

    Article  PubMed  Google Scholar 

  • Li Z, Deutscher MP (1996) Maturation pathways for E. coli tRNA precursors: a random multienzyme process in vivo. Cell 86:503–512

    Article  PubMed  CAS  Google Scholar 

  • Ma Y, Pannicke U, Schwarz K, Lieber MR (2002) Hairpin opening and overhang processing by an Artemis/DNA-dependent protein kinase complex in nonhomologous end joining and V(D)J recombination. Cell 108(6):781–794

    Article  PubMed  CAS  Google Scholar 

  • Mader U, Zig L, Kretschmer J, Homuth G, Putzer H (2008) mRNA processing by RNases J1 and J2 affects Bacillus subtilis gene expression on a global scale. Mol Microbiol 70(1):183–196

    Article  PubMed  Google Scholar 

  • Madhugiri R, Evguenieva-Hackenberg E (2009) RNase J is involved in the 5′-end maturation of 16 S rRNA and 23 S rRNA in Sinorhizobium meliloti. FEBS Lett 583(14):2339–2342

    Article  PubMed  CAS  Google Scholar 

  • Mandel CR, Kaneko S, Zhang H, Gebauer D, Vethantham V, Manley JL, Tong L (2006) Polyadenylation factor CPSF-73 is the pre-mRNA 3′-end-processing endonuclease. Nature 444(7121):953–956

    Article  PubMed  CAS  Google Scholar 

  • Mathy N, Benard L, Pellegrini O, Daou R, Wen T, Condon C (2007) 5′-to-3′ exoribonuclease activity in bacteria: role of RNase J1 in rRNA maturation and 5′ stability of mRNA. Cell 129(4):681–692

    Article  PubMed  CAS  Google Scholar 

  • Mathy N, Hebert A, Mervelet P, Benard L, Dorleans A, de la Sierra-Gallay IL, Noirot P, Putzer H, Condon C (2010) Bacillus subtilis ribonucleases J1 and J2 form a complex with altered enzyme behaviour. Mol Microbiol 75(2):489–498

    Article  PubMed  CAS  Google Scholar 

  • Minagawa A, Takaku H, Takagi M, Nashimoto M (2004) A novel endonucleolytic mechanism to generate the CCA 3′ termini of tRNA molecules in Thermotoga maritima. J Biol Chem 279(15):15688–15697

    Article  PubMed  CAS  Google Scholar 

  • Mir-Montazeri B, Ammelburg M, Forouzan D, Lupas AN, Hartmann MD (2010) Crystal structure of a dimeric archaeal cleavage and polyadenylation specificity factor. J Struct Biol. doi:10.1016/j.jsb.2010.09.013

    PubMed  Google Scholar 

  • Mowry KL, Steitz JA (1987) Identification of the human U7 snRNP as one of several factors involved in the 3′ end maturation of histone premessenger RNA’s. Science 238(4834):1682–1687

    Article  PubMed  CAS  Google Scholar 

  • Nishida Y, Ishikawa H, Baba S, Nakagawa N, Kuramitsu S, Masui R (2010) Crystal structure of an archaeal cleavage and polyadenylation specificity factor subunit from Pyrococcus horikoshii. Proteins 78(10):2395–2398

    Article  PubMed  CAS  Google Scholar 

  • Perwez T, Kushner SR (2006) RNase Z in Escherichia coli plays a significant role in mRNA decay. Mol Microbiol 60(3):723–737

    Article  PubMed  CAS  Google Scholar 

  • Pillai RS, Will CL, Luhrmann R, Schumperli D, Muller B (2001) Purified U7 snRNPs lack the Sm proteins D1 and D2 but contain Lsm10, a new 14 kDa Sm D1-like protein. EMBO J 20(19):5470–5479

    Article  PubMed  CAS  Google Scholar 

  • Pillai RS, Grimmler M, Meister G, Will CL, Luhrmann R, Fischer U, Schumperli D (2003) Unique Sm core structure of U7 snRNPs: assembly by a specialized SMN complex and the role of a new component, Lsm11, in histone RNA processing. Genes Dev 17(18):2321–2333

    Article  PubMed  CAS  Google Scholar 

  • Proudfoot NJ (1989) How RNA polymerase II terminates transcription in higher eukaryotes. Trends Biochem Sci 14(3):105–110

    Article  PubMed  CAS  Google Scholar 

  • Redko Y, Li de la Sierra-Gallay I, Condon C (2007) When all’s zed and done: the structure and function of RNase Z in prokaryotes. Nat Rev Microbiol 5(4):278–286

    Article  PubMed  CAS  Google Scholar 

  • Ryan K, Calvo O, Manley JL (2004) Evidence that polyadenylation factor CPSF-73 is the mRNA 3′ processing endonuclease. RNA 10(4):565–573

    Article  PubMed  CAS  Google Scholar 

  • Scharl EC, Steitz JA (1994) The site of 3′ end formation of histone messenger RNA is a fixed distance from the downstream element recognized by the U7 snRNP. EMBO J 13(10):2432–2440

    PubMed  CAS  Google Scholar 

  • Schiffer S, Helm M, Theobald-Dietrich A, Giege R, Marchfelder A (2001) The plant tRNA 3′ processing enzyme has a broad substrate spectrum. Biochemistry 40(28):8264–8272

    Article  PubMed  CAS  Google Scholar 

  • Schiffer S, Rosch S, Marchfelder A (2002) Assigning a function to a conserved group of proteins: the tRNA 3′- processing enzymes. EMBO J 21(11):2769–2777

    Article  PubMed  CAS  Google Scholar 

  • Schilling O, Ruggeberg S, Vogel A, Rittner N, Weichert S, Schmidt S, Doig S, Franz T, Benes V, Andrews SC, Baum M, Meyer-Klaucke W (2004) Characterization of an Escherichia coli elaC deletion mutant. Biochem Biophys Res Commun 320(4):1365–1373

    Article  PubMed  CAS  Google Scholar 

  • Schilling O, Spath B, Kostelecky B, Marchfelder A, Meyer-Klaucke W, Vogel A (2005) Exosite modules guide substrate recognition in the ZiPD/ElaC protein family. J Biol Chem 280(18):17857–17862

    Article  PubMed  CAS  Google Scholar 

  • Seidman JG, Schmidt FJ, Foss K, McClain WH (1975) A mutant of Escherichia coli defective in removing 3′ terminal nucleotides from some transfer RNA precursor molecules. Cell 5(4):389–400

    Article  PubMed  CAS  Google Scholar 

  • Shibata HS, Minagawa A, Takaku H, Takagi M, Nashimoto M (2006) Unstructured RNA is a substrate for tRNase Z. Biochemistry 45(17):5486–5492

    Article  PubMed  CAS  Google Scholar 

  • Spath B, Schubert S, Lieberoth A, Settele F, Schutz S, Fischer S, Marchfelder A (2008) Two archaeal tRNase Z enzymes: similar but different. Arch Microbiol 190(3):301–308

    Article  PubMed  Google Scholar 

  • Tavtigian SV, Simard J, Teng DH, Abtin V, Baumgard M, Beck A, Camp NJ, Carillo AR, Chen Y, Dayananth P, Desrochers M, Dumont M, Farnham JM, Frank D, Frye C, Ghaffari S, Gupte JS, Hu R, Iliev D, Janecki T, Kort EN, Laity KE, Leavitt A, Leblanc G, McArthur-Morrison J, Pederson A, Penn B, Peterson KT, Reid JE, Richards S, Schroeder M, Smith R, Snyder SC, Swedlund B, Swensen J, Thomas A, Tranchant M, Woodland AM, Labrie F, Skolnick MH, Neuhausen S, Rommens J, Cannon-Albright LA (2001) A candidate prostate cancer susceptibility gene at chromosome 17p. Nat Genet 27(2):172–180

    Article  PubMed  CAS  Google Scholar 

  • Uguen P, Murphy S (2003) The 3′ ends of human pre-snRNAs are produced by RNA polymerase II CTD-dependent RNA processing. EMBO J 22(17):4544–4554

    Article  PubMed  CAS  Google Scholar 

  • Walther TN, Wittop Koning TH, Schumperli D, Muller B (1998) A 5′-3′ exonuclease activity involved in forming the 3′ products of histone pre-mRNA processing in vitro. RNA 4(9):1034–1046

    Article  PubMed  CAS  Google Scholar 

  • Yang XC, Sullivan KD, Marzluff WF, Dominski Z (2009) Studies of the 5′ exonuclease and endonuclease activities of CPSF-73 in histone pre-mRNA processing. Mol Cell Biol 29(1):31–42

    Article  PubMed  Google Scholar 

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Acknowledgments

This work was supported by funds from the CNRS (UPR 9073), Université Paris VII-Denis Diderot and the Agence Nationale de la Recherche (ANR- SubtilRNA2). I thank colleagues and current and former lab members for their contributions to the data discussed in this chapter. I also thank Béatrice Clouet-d’Orval, Zbigniew Dominski, and Allen Nicholson for their helpful comments on the manuscript.

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Correspondence to Ciarán Condon .

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Condon, C., Gilet, L. (2011). The Metallo-β-Lactamase Family of Ribonucleases. In: Nicholson, A. (eds) Ribonucleases. Nucleic Acids and Molecular Biology. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-21078-5_10

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